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Original Research Communications |
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: We examined the relation of circumference (waist and hip) and skinfold-thickness (subscapular and triceps) measurements to lipid and insulin concentrations among 2996 children and adolescents aged 5–17 y.
Design: This was a community-based, cross-sectional study conducted in 1992–1994.
Results: A central or abdominal distribution of body fat was related to adverse concentrations of triacylglycerol, LDL cholesterol, HDL cholesterol, and insulin; these associations were independent of race, sex, age, weight, and height. These associations were observed whether fat patterning was characterized by using 1) waist circumference alone (after adjustment for weight and height), 2) waist-to-hip ratio, or 3) principal components analysis. Compared with a child at the 10th percentile of waist circumference, a child at the 90th percentile was estimated to have, on average, higher concentrations of LDL cholesterol (0.17 mmol/L), triacylglycerol (0.11 mmol/L), and insulin (6 pmol/L) and lower concentrations of HDL cholesterol (-0.07 mmol/L). These differences, which were independent of weight and height, were significant at the 0.001 level and were consistent across race-sex groups.
Conclusions: These findings emphasize the importance of obtaining information on body fat distribution, waist circumference in particular, in children. Waist circumference, which is relatively easy to measure, may help to identify children likely to have adverse concentrations of lipids and insulin.
Key Words: Fat distribution • children • lipids • insulin • waist circumference • hip circumference • skinfold thickness • body weight • Bogalusa Heart Study
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In contrast with these findings in adults, the importance of fat distribution in early life is less certain. Various fat patterns have been associated with concentrations of lipids and insulin and with blood pressure in some studies (9–14), but equivocal or negative results have also been reported (15–19); it is also possible that fat patterning is associated with risk factors only after sexual maturation (17). The study of fat distribution among children and adolescents can be difficult because there are marked changes in circumferences (20), skinfold thicknesses (21), and lipoprotein concentrations (22) during growth and development. Furthermore, the amount of intraabdominal fat, which may have a primary role in adverse health outcomes (6, 23–25), is small before adulthood (26, 27).
We showed previously, in 388 children with extreme (high or low) concentrations of LDL and VLDL cholesterol, that truncal skinfold thicknesses and waist circumference are related to concentrations of lipids and insulin (9, 10). The current analyses, which also included hip circumference, further examined these associations in a larger (n = 2996), representative sample of school-aged children. The goal of the present study was to determine whether information on skinfold thicknesses (subscapular and triceps) and circumferences (waist and hip) can improve the prediction of lipid and insulin concentrations among children and adolescents if weights and heights are already known.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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43000. Since 1973, cross-sectional studies of the school-age population have been conducted every 3–5 y; the current analysis consists of 5–17-y-olds who participated in the examination conducted between October 1992 and June 1994. Participation rates in previous cross-sectional studies ranged from 80% to 93% (28). Informed consent was obtained from all participants, and study protocols were approved by human subjects review committees of the Louisiana State University School of Medicine and the Tulane University School of Public Health and Tropical Medicine. Of the 3135 participants, we excluded 9 girls who reported that they were pregnant and 17 children who were missing one or more anthropometric measurements. We also excluded 7 children whose race-ethnicity was reported as other than white or black; the race-ethnicity of the mother was used for these classifications. Of the remaining 3102 children, cholesterol (total, LDL, and HDL) determinations were available for 2996. Analyses of triacylglycerol and insulin concentrations excluded an additional 347 children who reported not having fasted; another 133 children did not have a sample available for insulin determinations. The resulting sample sizes in the present analyses were 2516 (insulin), 2649 (triacylglycerol), and 2996 (LDL and HDL cholesterol). Although we observed a weak, positive association (that was significant at the 0.01 level) between waist circumference and concentrations of total cholesterol, these data are not presented because of the opposite associations of LDL and HDL cholesterol with the obesity indexes.
General examinations
Height was measured twice to the nearest 0.1 cm with a manual height board, and weight was measured twice to the nearest 0.1 kg with a balance-beam metric scale. No adjustments were made for the weight of the gown, underpants, or socks worn during the examination.
Each skinfold thickness and circumference was measured 3 times. The triceps and subscapular skinfold thicknesses were measured to the nearest millimeter with Lange skinfold calipers (Cambridge Scientific Industries, Inc, Cambridge, MD) and circumferences were measured with a nonstretchable tape. The subscapular skinfold thickness was measured immediately below the inferior angle of the scapula, waist circumference was measured midway between the rib cage and the superior border of the iliac crest, and hip circumference was measured at the greater trochanters. The mean value for each anthropometric characteristic was used in all analyses. The subscapular-to-triceps skinfold-thickness ratio (STR) and the waist-to-hip ratio (WHR), 2 widely used indexes of fat distribution, were also examined.
On each of the 262 screening days during the 21 mo of data collection, a 10% random sample of the examined children was selected to assess reproducibility. Intraclass (within-observer) correlation coefficients, based on pairs of measurements made by the same examiner on the same day, were >0.99 for height, weight, Quetelet index (in kg/m2), Rohrer index (in kg/m3), and hip circumference; 0.98 for each skinfold thickness; and 0.97 for waist circumference. The slightly lower reproducibility for the waist circumference was in part due to duplicate measurements (of 52 and 83 cm) for a 12-y-old with a Quetelet index of 28.9; excluding this girl increased the intraclass correlation coefficient to 0.98. No information is available for interobserver reproducibility because the original and repeat measurements were made by the same examiner.
Because the stage of sexual maturation is associated with fat distribution (21) and lipid concentrations (22), an index of sexual development was included in some analyses. Maturation was determined by a physician according to the 5 categories of Tanner (29); this classification was based on a combination of the appearance of female breast or male genitalia and pubic hair development.
Laboratory analyses
Concentrations of serum cholesterol and triacylglycerol were measured, in the Bogalusa Heart Study Core Laboratory, by enzymatic procedures (Abbott VP, North Chicago) (30, 31). The laboratory met the performance requirements of the Centers for Disease Control and Prevention (CDC) Lipid Standardization Program and is monitored by this program for the accuracy of total cholesterol, triacylglycerol, and HDL-cholesterol measurements. Measurements of LDL and HDL cholesterol were made with a combination of heparin-calcium precipitation and agar-agarose gel electrophoresis (32). Plasma insulin concentrations were measured in the centralized laboratory by a radioimmunoassay procedure (Phaadebas Insulin Kit; Pharmacia Diagnostics AB, Piscataway, NJ).
CDC-assigned quality control samples were used to monitor the cholesterol and triacylglycerol analyses, and the accuracy was well within the limits set by this agency. In addition, a 10% sample was randomly chosen each day to assess measurement error, and with the exception of insulin concentrations (0.91), intraclass correlation coefficients ranged from 0.95 (HDL cholesterol) to 0.995 (triacylglycerol). Median concentrations of the laboratory determinations, along with the overall 10th and 90th percentiles, are shown in Table 1
. Lipid and insulin concentrations differed substantially by race, sex, and age.
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Race, sex, age, and height were treated as covariates in all analyses, and weight was included in analyses that examined whether the circumferences and skinfold thicknesses provided additional (independent) information on risk factors. Although we also included the Quetelet or Rohrer index in some regression models, it may be more appropriate to adjust for weight and height separately (7); furthermore, although the Quetelet index is widely used as a measure of relative weight (35), it is moderately correlated with height in schoolchildren (r = 0.55 in the current study).
Because of the differences in scale of the anthropometric dimensions, predicted differences in risk factors are presented for children at the 10th and 90th percentiles of each skinfold thickness or circumference. Furthermore, because of the difficulty in interpreting regression coefficients in the presence of highly correlated variables, several statistical tests were based on whether a set of regression coefficients was equal to 0 (chunk tests), and therefore provided no additional information on the outcome. Several results were verified by using least-trimmed squares regression; whereas ordinary least-squares regression minimizes the sum of all squared deviations, this robust method minimizes 50% of the squared deviations and provided a good fit for the bulk of the data (36).
Although ratios are widely used in studies of body fat distribution, to adequately correct for the characteristic in the denominator, it is necessary for a regression of the numerator on the denominator to have a y intercept of 0 (37, 38); furthermore, the use of WHR is analogous to modeling an interaction (without main effects) between waist and hip-1 in regression models. We therefore focused on the individual characteristics and used principal components analysis to reduce the 4 measurements (2 circumferences and 2 skinfold thicknesses) to a smaller number of uncorrelated variables (4, 39). Residuals from a regression of the circumferences and skinfold thicknesses on race, sex, age, weight, and height were used in these analyses and we found the first principal component to be positively correlated (r: 0.5–0.9) with all anthropometric dimensions, reflecting the overall level of obesity. The second component contrasted the waist circumference with the hip circumference and triceps skinfold thickness and was interpreted as an index of central fat distribution.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) was strongly associated with age, and thicknesses were consistently higher in girls than in boys and in white boys than in black boys. The relation of the triceps skinfold thickness to age differed substantially by sex: during adolescence, thicknesses either remained stable or increased slightly among girls, whereas they decreased by 20–40% among boys. Smaller race-sex differences were seen for the circumferences, but white boys had the largest waist girths. Because the increase with age was proportionately greater for hip circumference than for waist circumference, mean WHRs decreased from 0.86 (age 5 y) to 0.75 (age 17 y) among girls and from 0.87 to 0.82 among boys (data not shown).
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). The Quetelet index was related strongly to the individual circumference (r: 0.9) and skinfold-thickness (r: 0.8) measures; waist and hip circumferences were also strongly associated with each other and with the skinfold thicknesses (r: 0.8–0.9). In contrast, a weaker correlation (r = 0.35) was seen between WHR and STR, suggesting that each might capture a different aspect of fat distribution. Adjustment for weight substantially reduced the magnitudes of most associations (values in parentheses); the largest decrease was seen in the correlation between waist and hip circumferences.
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). For example, compared with a child at the 10th percentile of weight, a child (of the same sex, race, age, and height) at the 90th percentile of weight was estimated to have a 0.30-mmol/L higher LDL-cholesterol concentration, a 0.32-mmol/L higher triacylglycerol concentration, a 0.19-mmol/L lower HDL-cholesterol concentration, and a 54-pmol/L higher insulin concentration. Predicted differences in LDL-cholesterol concentrations varied little across the individual anthropometric dimensions, with increases ranging from 0.30 mmol/L (weight and hip circumference) to 0.34 mmol/L (subscapular skinfold thickness); differences across deciles of WHR and STR tended to be smaller. Predicted changes in other risk factors also varied only slightly across the individual anthropometric dimensions: for triacylglycerol, from 0.29 to 0.34 mmol/L; for HDL cholesterol, from -0.16 to -0.20 mmol/L; and for insulin, from 43 to 54 pmol/L. In general, the weakest associations were seen with triceps skinfold thickness.
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). This specific relation is shown because age was weakly related to concentrations of HDL cholesterol (r = -0.09) and Rohrer index (r = 0.01) among girls; results were similar among black and white girls. Although there were some inconsistencies within the 9 strata shown in Figure 2, an increase in waist circumference from 60 to 80 cm was typically associated with a decrease in HDL-cholesterol concentration of from 0.15 to 0.25 mmol/L. Furthermore, these associations did not differ significantly by relative weight or age; among 5–9-y-old black girls, for example, a 20-cm increase in waist circumference was independently associated with a 0.36-mmol/L decrease in HDL cholesterol (data not shown). Additional regression models indicated that independently of the Rohrer index, a 20-cm increase in waist circumference among black girls was also associated with increases of 0.16 mmol/L in triacylglycerol and 57 pmol/L in insulin, but little difference in concentrations of LDL cholesterol.
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). For example, a child with a waist circumference at the 90th percentile was estimated to have a 0.17-mmol/L higher LDL-cholesterol concentration than a child at the 10th percentile. (Similar results were obtained by using least-trimmed squares rather than ordinary least-squares.) Compared with the previous results, the smaller predicted differences shown in Table 4 were largely due to the reduced variability of the anthropometric dimensions after adjustment for weight. (The decreased variability in waist circumference after stratification by Rohrer index is evident in Figure 2
.) Predicted changes across subscapular skinfold thicknesses were fairly similar to those seen with waist circumference, but associations with hip circumference and triceps skinfold thickness were small and inconsistent. Spearman correlation coefficients also indicated that associations were generally strongest for waist circumference and subscapular skinfold thickness and weakest for hip circumference.
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, additional analyses indicated that weight provided no additional information on concentrations of LDL cholesterol, triacylglycerol, or HDL cholesterol if waist circumference (in addition to race, sex, age, and height) was known (partial /r/ 
0.04). Weight, however, did improve the prediction of insulin concentrations beyond that achieved with waist circumference.
Forward stepwise regression was then used to determine which circumferences and skinfold thicknesses were most predictive of risk factor concentrations if weight and other covariates were known (Table 5). Of the 4 measures, waist circumference was consistently associated with concentrations of each risk factor; other predictors (at the 0.01 level) included subscapular skinfold thickness and hip circumference. Hip circumference, however, was significantly related to concentrations of triacylglycerol and HDL cholesterol only if circumference was also included in the regression models. Triceps skinfold thickness did not provide independent information on any outcome.
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are the corresponding results for the ratios and principal components. These analyses indicated that the second principal component, which was associated positively (r: 0.8) with waist circumference and inversely (r: -0.35) with both hip circumference and triceps skinfold thickness, was associated with adverse concentrations of all risk factors. Furthermore, this index of central fat patterning was uncorrelated with the first component (general degree of obesity) and showed moderate to strong correlations with the adjusted waist circumference (r: 0.74), WHR (r: 0.68), and STR (r: 0.42).
In general, associations with risk factors differed only slightly across race and sex groups (Table 6). As assessed by product terms in regression models, the only significant differences (at the 0.001 level) in the associations with fat patterning were that the strength of the relation of WHR to concentrations of both LDL cholesterol and triacylglycerol increased with age. Among 5–9-y-olds, for example, a child with an adverse (90th percentile) WHR had, on average, a (nonsignificant) 0.03-mmol/L lower LDL-cholesterol concentration and a 0.02-mmol/L higher triacylglycerol concentration than did a child at the 10th percentile. An inverse association between waist circumference and concentrations of HDL cholesterol, however, was evident even among the 5–9-y-olds.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Waist circumference showed the most consistent, and generally strongest, associations with adverse risk factor concentrations. These findings likely reflect the ability of waist circumference to function as an index of both fat distribution and generalized obesity, as well as the relation of waist circumference with correlates of lipid concentrations. For example, waist circumference was strongly associated with age and Quetelet index and circumferences differed between boys and girls and between white boys and black boys. Because waist circumference is also relatively easy to measure, it may be particularly appropriate for epidemiologic studies of children. Race-, sex-, and age-specific 50th and 90th percentiles for waist circumference based on the current sample are shown in Table 7. This information may help in the identification of persons who are likely to have adverse lipid and insulin concentrations.
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It has been suggested that the amount of intraabdominal fat is the primary determinant of adverse outcomes (6, 23–25) and that the lipolysis of intraabdominal adipocytes may lead to high concentrations of fatty acids (24). However, various metabolic outcomes are also associated with chest circumference (42) and truncal subcutaneous adipose tissue (43). In agreement with our observation that triacylglycerol concentrations are independently related to both waist circumference and subscapular skinfold thickness (Table 5), WHR and STR have also been found to be independent predictors of triacylglycerol concentrations among adults (44). These associations with various fat patterns suggest that it may be difficult to identify the best anthropometric index of fat distribution, which may also vary by outcome and population (45). It would be helpful if additional studies were performed to determine whether intraabdominal fat is the primary determinant of adverse health outcomes; adequate statistical control of the overall degree of obesity would be important in the analyses of these data.
Studies of fat patterning in children are further complicated by the 1) small amount of intraabdominal fat present before adulthood (26, 27) and 2) the rapid changes in fat patterning that occur during growth and development (21). It is also likely that some anthropometric indexes of fat distribution among adults, such as WHR, may be inappropriate for children and adolescents. For example, the proportionately larger increases in hip (compared with waist) circumference that we and others (20) observed during growth may account for the low correlation between WHR and intraabdominal fat among adolescents (12, 14, 26). Furthermore, to adequately correct for the characteristic in the denominator of a ratio such as WHR, a regression of the numerator on the denominator should have a y intercept of 0 (37, 38); in contrast, the regression line in the current study was waist circumference = 3.4 + 0.78 x hip circumference. Other investigations of children and adults have also suggested that waist circumference (7, 8, 13, 26) or various skinfold thicknesses (12, 27, 43) may be better measures of fat distribution than is WHR.
Several limitations of the current study should be considered. Only 2 skinfold thicknesses and 2 circumferences were obtained and it is possible that measurements at other sites [such as at the chest or thigh (4, 42, 46, 47)] may have provided additional information. Although the optimal sites are uncertain, small changes in the location of the waist measurement can influence associations with risk factors (42); the associations with STR in the current study were influenced by the low precision of skinfold-thickness ratios (48). Furthermore, the current analyses used fasting insulin concentrations as a surrogate for insulin resistance, and as assessed by whole-body glucose uptake in clamp studies, there is only a moderately strong correlation (r = 0.65–0.70) between the 2 measurements (49).
Despite these limitations, our findings may have important implications for the choice of skinfold-thickness or circumference measurements in clinical and epidemiologic studies. Whereas waist circumference, which is relatively easy to measure, appears to be an important correlate of concentrations of lipids and insulin among children and adolescents, triceps skinfold thickness and hip circumference provide little additional information about risk factors if weight and height are known. These findings suggest that the measurement of waist circumference may help to identify children and adolescents with adverse concentrations of lipids and other risk factors. These persons could then targeted for weight reduction and risk-factor surveillance.
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FOOTNOTES |
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2 Supported by grants HL 15103 and HL 32194 from the National Heart, Lung, and Blood Institute, National Institutes of Health, and by funds from the CDC and Robert W. Woodruff Foundations.
3 Address reprint requests to DS Freedman, CDC Mailstop K-26, 4770 Buford Highway, Atlanta, GA 30341-3717. E-mail: Dxf1{at}Cdc.gov.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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